A dehydrin-dehydrin interaction: The case of SK3 from Opuntia streptacantha

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Hernández Sánchez, Itzell E ^a   Martynowicz, David M ^b   Rodríguez Hernández, Aida A ^a   Pérez Morales, Maria B ^a   Graether, Steffen P ^b   Jiménez Bremont, Juan F ^a  

^a INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Histidine rich region; Homodimer; Intrinsically disordered proteins; K segments; SK3 dehydrin; Yeast two hybrid

Indexed keywords

EID: 84908008827     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00520     Document Type: Article

References (46)

1. Allagulova R., Gimalov, F. R., Shakirova, F. M., and Vakhitov, V. A. (2003). The plant dehydrins: structure and putative functions. Biochemistry Mosc. 68, 945–951. doi:10.1023/A:1026077825584
2. Andrews, P. (1970). Estimation of molecular size and molecular weights of biological compounds by gel filtration. Methods Biochem. Anal. 18, 1–53. doi:10.1002/9780470110362.ch1
3. Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., and Covarrubias, A. A. (2008). The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 148, 6–24. doi:10.1104/pp.108.120725
4. Close, T. J. (1996). Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Planta 97, 795–803. doi:10.1111/j.1399-3054.1996.tb00546.x
5. Close, T. J. (1997). Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol. Planta 100, 291–296. doi:10.1111/j.1399-3054.1997.tb04785.x
6. DeVincenzi, D. L., and Hedrick, J. L. (1967). Reevaluation of the molecular weights of glycogen phosphorylases a and b using Sephadex gel filtration. Biochemistry 6, 3489–3497. doi:10.1021/bi00863a021
7. Drira, M., Saibi, W., Brini, F., Gargouri, A., Masmoudi, K., and Hanin, M. (2013). The K-segments of the wheat dehydrin DHN-5 are essential for the protection of lactate dehydrogenase and β-glucosidase activities in vitro. Mol. Biotechnol. 54, 643–650. doi:10.1007/s12033-012-9606-8
8. Eriksson, S. K., Kutzer, M., Procek, J., Gröbner, G., and Harryson, P. (2011). Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell 23, 2391–2404. doi:10.1105/tpc.111.085183
9. Findlater, E. E., and Graether, S. P. (2009). NMR assignments of the intrinsically disordered K2 and YSK2 dehydrins. Biomol. NMR Assign. 3, 73–275. doi:10.1007/s12104-009-9192-2
10. Goto, S. G. (2001). A novel gene that is up-regulated during recovery from cold shock in Drosophila melanogaster. Gene 270, 259–264. doi:10.1016/S0378-1119(01)00465-6
11. Gsponer, J., Futschik, M. E., Teichmann, S. A., and Babu, M. M. (2008). Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322, 1365–1368. doi:10.1126/science.1163581
12. Hanin, M., Brini, F., Ebel, C., Toda, Y., and Takeda, S. (2011). Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal. Behav. 6, 1503–1509. doi:10.4161/psb.6.10.17088
13. Hara, M. (2010). The multifunctionality of dehydrins: an overview. Plant Signal. Behav. 5, 503–508. doi:10.4161/psb.11085
14. Hara, M., Fujinaga, M., and Kuboi, T. (2005). Metal binding by citrus dehydrin with histidine-rich domains. J. Exp. Bot. 56, 2695–2703. doi:10.1093/jxb/eri262
15. Hara, M., Kondo, M., and Kato, T. (2013). A KS-type dehydrin and its related domains reduce Cu-promoted radical generation and the histidine residues contribute to the radical-reducing activities. J. Exp. Bot. 64, 1615–1624. doi:10.1093/jxb/ert016
16. Hara, M., Shinoda, Y., Tanaka, Y., and Kuboi, T. (2009). DNA binding of citrus dehydrin promoted by zinc ion. Plant Cell Environ. 32, 532–541. doi:10.1111/j.1365-3040.2009.01947.x
17. Hara, M., Terashima, S., Fukaya, T., and Kuboi, T. (2003). Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 17, 290–298. doi:10.1007/s00425-003-0986-7
18. Hara, M., Terashima, S., and Kuboi, T. (2001). Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J. Plant Physiol. 158, 1333–1339. doi:10.1078/0176-1617-00600
19. Hincha, D. K., and Thalhammer, A. (2012). LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem. Soc. Trans. 40, 1000–1003. doi:10.1042/BST20120109
20. Hughes, S., and Graether, S. P. (2011). Cryoprotective mechanism of a small intrinsically disordered dehydrin protein. Prot. Sci. 20, 42–50. doi:10.1002/pro.534
21. Hughes, S. L., Schart, V., Malcolmson, J., Hogarth, K. A., Martynowicz, D. M., Tralman-Baker, E., et al. (2013). The importance of size and disorder in the cryoprotective effects of dehydrins. Plant Physiol. 163, 1376–1386. doi:10.1104/pp.113.226803
22. Jiménez-Bremont, J. F., Maruri-López, I., Ochoa-Alfaro, A. E., Delgado-Sánchez, P., Bravo, J., and Rodríguez-Kessler, M. (2013). LEA gene introns: is the intron of dehydrin genes a characteristic of the serine-segment? Plant Mol. Biol. Rep. 31, 128–140. doi:10.1007/S11105-012-0483-X
23. Koag, M. C., Fenton, R. D., Wilkens, S., and Close, T. J. (2003). The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol. 131, 309–316. doi:10.1104/pp.011171
24. Koag, M. C., Wilkens, S., Fenton, R. D., Resnik, J., Vo, E., and Close, T. J. (2009). The K-Segment of maize DHN1 mediumtes binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol. 150, 503–1514. doi:10.1104/pp.109.136697
25. Kovacs, D., Kalmar, E., Torok, Z., and Tompa, P. (2008). Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol. 147, 381–390. doi:10.1104/pp.108.118208
26. Livernois, A. M., Hnatchuk, D. J., Findlater, E. E., and Graether, S. P. (2009). Obtaining highly purified intrinsically disordered protein by boiling lysis and single step ion exchange. Anal. Biochem. 392, 70–76. doi:10.1016/j.ab.2009.05.023
27. Marchesseau, S., Mani, J. C., Martineau, P., Roquet, F., Cuq, J. L., and Pugnière, M. (2002). Casein interactions studied by the surface plasmon resonance technique. J. Dairy Sci. 85, 2711–2721. doi:10.3168/jds.S0022-0302(02)74358-0
28. Möckli, N., and Auerbach, D. (2004). Quantitative β-galactosidase assay suitable for high-throughput applications in the yeast two-hybrid system. BioTechniques 36, 872–876.
29. Möckli, N., Deplazes, A., and Auerbach, D. (2008). Finding new protein interactions using the DUALhunter system. Nat. Methods. Available online at: http://www.nature.com/nmeth/journal/v5/n2/abs/nmeth.f.204.html
30. Mouillon, J. M., Eriksson, S. K., and Harryson, P. (2008). Mimicking the plant cell interior under water stress by macromolecular crowding: disordered dehy-drin proteins are highly resistant to structural collapse. Plant Physiol. 148, 1925–1937. doi:10.1104/pp.108.124099
31. 3 dehydrin isolated from an Opuntia streptacantha cDNA library. Planta 235, 565–578. doi:10.1007/s00425-011-1531-8
32. Parmar, A. S., and Muschol, M. (2009). Hydration and hydrodynamic interactions of lysozyme: effects of chaotropic versus kosmotropic ions. Biophys. J. 97, 590–598. doi:10.1016/j.bpj.2009.04.045
33. Peng, Y., Reyes, J. L., Wei, H., Yang, Y., Karlson, D., Covarrubias, A. A., et al. (2008). RcDhn5, a cold acclimationresponsive dehydrin from Rhododendron cataw-biense rescues enzyme activity from dehydration effects in vitro and enhances freezing tolerance in RcDhn5-overexpressing Arabidopsis plants. Physiol. Plant. 134, 583–597. doi:10.1111/j.1399-3054.2008.01164.x
34. Potschka, M. (1987). Universal calibration of gel permeation chromatography and determination of molecular shape in solution. Anal. Biochem. 162, 47–64.
35. Rahman, L. N., Chen, L., Nazim, S., Bamm, V. V., Yaish, M. W., Moffatt, B. A., et al. (2010). Interactions of intrinsically disordered Thellungiella salsuginea dehy-drins TsDHN-1 and TsDHN-2 with membranes - synergistic effects of lipid composition and temperature on secondary structure. Biochem. Cell Biol. 88, 791–807. doi:10.1139/O10-026
36. Rahman, L. N., McKay, F., Giuliani, M., Quirk, A., Moffatt, B. A., Harauz, G., et al. (2013). Interactions of Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes at cold and ambient temperatures—surface morphology and single-molecule force measurements show phase separation, and reveal tertiary and quaternary associations. Biochim. Biophys. Acta 1828, 967–980. doi:10.1016/j.bbamem.2012.11.031
37. Reyes, J. L., Campos, F., Wei, H. U. I., Arora, R., Yang, Y., Karlson, D. T., et al. (2008). Functional dissection of Hydrophilins during in vitro freeze protection. Plant Cell Environ. 31, 1781–1790. doi:10.1111/j.1365-3040.2008.01879.x
38. Soulages, J. L., Kim, K., Arrese, E. L., Walters, C. and Cushman, J. C. (2003). Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (L-proline)-type II structure. Plant Physiol. 131, 963–975. doi:10.1104/pp.015891
39. Sun, X., and Lin, H. (2010). Role of plant dehydrins in antioxidation mechanisms. Biologia 65, 755–759. doi:10.2478/s11756-010-0090-y
40. Tompa, P. (2002). Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527–533. doi:10.1016/S0968-0004(02)02169-2
41. Tompa, P., Bánki, P., Bokor, M., Kamasa, P., Kovács, D., Lasanda, G. et al. (2006). Protein-water and Protein-buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR intensity and DSC aspects. Biophys. J. 91, 2243–2249. doi:10.1529/biophysj.106.084723
42. Tompa, P., and Kovacs, D. (2010). Intrinsically disordered chaperones in plants and animals. Biochem. Cell Biol. 88, 167–174. doi:10.1139/O09-163
43. Tunnacliffe, A., and Wise, M. J. (2007). The continuing conundrum of the LEA proteins. Naturwissenschaften 94, 791–812. doi:10.1007/s00114-007-0254-y
44. Uversky, V. N. (2002). Natively unfolded proteins: a point where biology waits for physics. Prot. Sci. 11, 739–756. doi:10.1110/ps.4210102
45. Xu, D. P., Duan, X. L., and Wang, B. Y. (1996). Expression of a late embryogenesis abundant protein gene HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110, 249–257.
46. 3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci. 170, 1164–1172. doi:10.1016/j.plantsci.2006.02.002